Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Dec 29;353(1378):2039–2061. doi: 10.1098/rstb.1998.0351

Molecular phylogeny of brachiopods and phoronids based on nuclear-encoded small subunit ribosomal RNA gene sequences

B LCohen
PMCID: PMC1692429

Abstract

Brachiopod and phoronid phylogeny is inferred from SSU rDNA sequences of 28 articulate and nine inarticulate brachiopods, three phoronids, two ectoprocts and various outgroups, using gene trees reconstructed by weighted parsimony, distance and maximum likelihood methods. Of these sequences, 33 from brachiopods, two from phoronids and one each from an ectoproct and a priapulan are newly determined. The brachiopod sequences belong to 31 different genera and thus survey about 10% of extant genus-level diversity. Sequences determined in different laboratories and those from closely related taxa agree well, but evidence is presented suggesting that one published phoronid sequence (GenBank accession UO12648) is a brachiopod-phoronid chimaera, and this sequence is excluded from the analyses. The chiton, Acanthopleura, is identified as the phenetically proximal outgroup; other selected outgroups were chosen to allow comparison with recent, non-molecular analyses of brachiopod phylogeny. The different outgroups and methods of phylogenetic reconstruction lead to similar results, with differences mainly in the resolution of weakly supported ancient and recent nodes, including the divergence of inarticulate brachiopod sub-phyla, the position of the rhynchonellids in relation to long- and short-looped articulate brachiopod clades and the relationships of some articulate brachiopod genera and species. Attention is drawn to the problem presented by nodes that are strongly supported by non-molecular evidence but receive only low bootstrap resampling support. Overall, the gene trees agree with morphology-based brachiopod taxonomy, but novel relationships are tentatively suggested for thecideidine and megathyrid brachiopods. Articulate brachiopods are found to be monophyletic in all reconstructions, but monophyly of inarticulate brachiopods and the possible inclusion of phoronids in the inarticulate brachiopod clade are less strongly established. Phoronids are clearly excluded from a sister-group relationship with articulate brachiopods, this proposed relationship being due to the rejected, chimaeric sequence (GenBank UO12648). Lineage relative rate tests show no heterogeneity of evolutionary rate among articulate brachiopod sequences, but indicate that inarticulate brachiopod plus phoronid sequences evolve somewhat more slowly. Both brachiopods and phoronids evolve slowly by comparison with other invertebrates. A number of palaeontologically dated times of earliest appearance are used to make upper and lower estimates of the global rate of brachiopod SSU rDNA evolution, and these estimates are used to infer the likely divergence times of other nodes in the gene tree. There is reasonable agreement between most inferred molecular and palaeontological ages. The estimated rates of SSU rDNA sequence evolution suggest that the last common ancestor of brachiopods, chitons and other protostome invertebrates (Lophotrochozoa and Ecdysozoa) lived deep in Precambrian time. Results of this first DNA-based, taxonomically representative analysis of brachiopod phylogeny are in broad agreement with current morphology-based classification and systematics and are largely consistent with the hypothesis that brachiopod shell ontogeny and morphology are a good guide to phylogeny.

Full Text

The Full Text of this article is available as a PDF (403.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adoutte A., Philippe H. The major lines of metazoan evolution: summary of traditional evidence and lessons from ribosomal RNA sequence analysis. EXS. 1993;63:1–30. doi: 10.1007/978-3-0348-7265-2_1. [DOI] [PubMed] [Google Scholar]
  2. Aguinaldo A. M., Turbeville J. M., Linford L. S., Rivera M. C., Garey J. R., Raff R. A., Lake J. A. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature. 1997 May 29;387(6632):489–493. doi: 10.1038/387489a0. [DOI] [PubMed] [Google Scholar]
  3. Allard M. W., Ellsworth D. L., Honeycutt R. L. The production of single-stranded DNA suitable for sequencing using the polymerase chain reaction. Biotechniques. 1991 Jan;10(1):24–26. [PubMed] [Google Scholar]
  4. Banta W. C., Backus B. T. 18S rDNA from lophophorates. Science. 1995 Dec 15;270(5243):1852–1852. [PubMed] [Google Scholar]
  5. Benson D. A., Boguski M. S., Lipman D. J., Ostell J. GenBank. Nucleic Acids Res. 1997 Jan 1;25(1):1–6. doi: 10.1093/nar/25.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buckler E. S., 4th, Ippolito A., Holtsford T. P. The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics. 1997 Mar;145(3):821–832. doi: 10.1093/genetics/145.3.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohen B. L., Stark S., Gawthrop A. B., Burke M. E., Thayer C. W. Comparison of articulate brachiopod nuclear and mitochondrial gene trees leads to a clade-based redefinition of protostomes (Protostomozoa) and deuterostomes (Deuterostomozoa) Proc Biol Sci. 1998 Mar 22;265(1395):475–482. doi: 10.1098/rspb.1998.0319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elwood H. J., Olsen G. J., Sogin M. L. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol Biol Evol. 1985 Sep;2(5):399–410. doi: 10.1093/oxfordjournals.molbev.a040362. [DOI] [PubMed] [Google Scholar]
  10. Field K. G., Olsen G. J., Lane D. J., Giovannoni S. J., Ghiselin M. T., Raff E. C., Pace N. R., Raff R. A. Molecular phylogeny of the animal kingdom. Science. 1988 Feb 12;239(4841 Pt 1):748–753. doi: 10.1126/science.3277277. [DOI] [PubMed] [Google Scholar]
  11. Guigó R., Muchnik I., Smith T. F. Reconstruction of ancient molecular phylogeny. Mol Phylogenet Evol. 1996 Oct;6(2):189–213. doi: 10.1006/mpev.1996.0071. [DOI] [PubMed] [Google Scholar]
  12. Halanych K. M., Bacheller J. D., Aguinaldo A. M., Liva S. M., Hillis D. M., Lake J. A. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science. 1995 Mar 17;267(5204):1641–1643. doi: 10.1126/science.7886451. [DOI] [PubMed] [Google Scholar]
  13. Halanych K. M., Bacheller J. D., Aguinaldo A. M., Liva S. M., Hillis D. M., Lake J. A. Response: lophophorate phylogeny. Science. 1996 Apr 12;272(5259):283–283. doi: 10.1126/science.272.5259.283. [DOI] [PubMed] [Google Scholar]
  14. Halanych K. M. The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Mol Phylogenet Evol. 1995 Mar;4(1):72–76. doi: 10.1006/mpev.1995.1007. [DOI] [PubMed] [Google Scholar]
  15. Hancock J. M. The contribution of slippage-like processes to genome evolution. J Mol Evol. 1995 Dec;41(6):1038–1047. doi: 10.1007/BF00173185. [DOI] [PubMed] [Google Scholar]
  16. Hasegawa M., Kishino H., Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22(2):160–174. doi: 10.1007/BF02101694. [DOI] [PubMed] [Google Scholar]
  17. Hendriks L., Van Broeckhoven C., Vandenberghe A., Van de Peer Y., De Wachter R. Primary and secondary structure of the 18S ribosomal RNA of the bird spider Eurypelma californica and evolutionary relationships among eukaryotic phyla. Eur J Biochem. 1988 Oct 15;177(1):15–20. doi: 10.1111/j.1432-1033.1988.tb14339.x. [DOI] [PubMed] [Google Scholar]
  18. Hillis D. M., Huelsenbeck J. P. Signal, noise, and reliability in molecular phylogenetic analyses. J Hered. 1992 May-Jun;83(3):189–195. doi: 10.1093/oxfordjournals.jhered.a111190. [DOI] [PubMed] [Google Scholar]
  19. Hillis D. M. Inferring complex phylogenies. Nature. 1996 Sep 12;383(6596):130–131. doi: 10.1038/383130a0. [DOI] [PubMed] [Google Scholar]
  20. Jaeger J. A., Turner D. H., Zuker M. Improved predictions of secondary structures for RNA. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7706–7710. doi: 10.1073/pnas.86.20.7706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jaeger J. A., Turner D. H., Zuker M. Predicting optimal and suboptimal secondary structure for RNA. Methods Enzymol. 1990;183:281–306. doi: 10.1016/0076-6879(90)83019-6. [DOI] [PubMed] [Google Scholar]
  22. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  23. Kumar S., Rzhetsky A. Evolutionary relationships of eukaryotic kingdoms. J Mol Evol. 1996 Feb;42(2):183–193. doi: 10.1007/BF02198844. [DOI] [PubMed] [Google Scholar]
  24. Lake J. A. Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1455–1459. doi: 10.1073/pnas.91.4.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mackey L. Y., Winnepenninckx B., De Wachter R., Backeljau T., Emschermann P., Garey J. R. 18S rRNA suggests that Entoprocta are protostomes, unrelated to Ectoprocta. J Mol Evol. 1996 May;42(5):552–559. doi: 10.1007/BF02352285. [DOI] [PubMed] [Google Scholar]
  26. McCallum F. S., Maden B. E. Human 18 S ribosomal RNA sequence inferred from DNA sequence. Variations in 18 S sequences and secondary modification patterns between vertebrates. Biochem J. 1985 Dec 15;232(3):725–733. doi: 10.1042/bj2320725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moore J., Willmer P. Convergent evolution in invertebrates. Biol Rev Camb Philos Soc. 1997 Feb;72(1):1–60. doi: 10.1017/s0006323196004926. [DOI] [PubMed] [Google Scholar]
  28. Morris S. C., Cohen B. L., Gawthrop A. P., Cavalier-Smith T., Winnepenninckx B. Lophophorate phylogeny. Science. 1996 Apr 12;272(5259):282–283. doi: 10.1126/science.272.5259.282. [DOI] [PubMed] [Google Scholar]
  29. Norell M. A., Novacek M. J. The fossil record and evolution: comparing cladistic and paleontologic evidence for vertebrate history. Science. 1992 Mar 27;255(5052):1690–1693. doi: 10.1126/science.255.5052.1690. [DOI] [PubMed] [Google Scholar]
  30. Olsen G. J., Woese C. R. Ribosomal RNA: a key to phylogeny. FASEB J. 1993 Jan;7(1):113–123. doi: 10.1096/fasebj.7.1.8422957. [DOI] [PubMed] [Google Scholar]
  31. Rice E. L., Roddick D., Singh R. K. A comparison of molluscan (Bivalvia) phylogenies based on palaeontological and molecular data. Mol Mar Biol Biotechnol. 1993 Jun;2(3):137–146. [PubMed] [Google Scholar]
  32. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  33. Sheen J. Y., Seed B. Electrolyte gradient gels for DNA sequencing. Biotechniques. 1988 Nov-Dec;6(10):942–944. [PubMed] [Google Scholar]
  34. Smith S. W., Overbeek R., Woese C. R., Gilbert W., Gillevet P. M. The genetic data environment an expandable GUI for multiple sequence analysis. Comput Appl Biosci. 1994 Dec;10(6):671–675. doi: 10.1093/bioinformatics/10.6.671. [DOI] [PubMed] [Google Scholar]
  35. Steiner G., Müller M. What can 18S rDNA do for bivalve phylogeny? J Mol Evol. 1996 Jul;43(1):58–70. doi: 10.1007/BF02352300. [DOI] [PubMed] [Google Scholar]
  36. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993 May;10(3):512–526. doi: 10.1093/oxfordjournals.molbev.a040023. [DOI] [PubMed] [Google Scholar]
  37. Van de Peer Y., Neefs J. M., De Rijk P., De Wachter R. Reconstructing evolution from eukaryotic small-ribosomal-subunit RNA sequences: calibration of the molecular clock. J Mol Evol. 1993 Aug;37(2):221–232. doi: 10.1007/BF02407359. [DOI] [PubMed] [Google Scholar]
  38. Van de Peer Y., Van der Auwera G., De Wachter R. The evolution of stramenopiles and alveolates as derived by "substitution rate calibration" of small ribosomal subunit RNA. J Mol Evol. 1996 Feb;42(2):201–210. doi: 10.1007/BF02198846. [DOI] [PubMed] [Google Scholar]
  39. Vogler A. P., Welsh A., Hancock J. M. Phylogenetic analysis of slippage-like sequence variation in the V4 rRNA expansion segment in tiger beetles (Cicindelidae). Mol Biol Evol. 1997 Jan;14(1):6–19. doi: 10.1093/oxfordjournals.molbev.a025703. [DOI] [PubMed] [Google Scholar]
  40. Winnepenninckx B., Backeljau T., De Wachter R. Complete small ribosomal subunit RNA sequence of the chiton Acanthopleura japonica (Lischke, 1873) (Mollusca, Polyplacophora). Nucleic Acids Res. 1993 Apr 11;21(7):1670–1670. doi: 10.1093/nar/21.7.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Winnepenninckx B., Backeljau T., De Wachter R. Phylogeny of protostome worms derived from 18S rRNA sequences. Mol Biol Evol. 1995 Jul;12(4):641–649. doi: 10.1093/oxfordjournals.molbev.a040243. [DOI] [PubMed] [Google Scholar]
  42. Yang Z. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol. 1994 Sep;39(3):306–314. doi: 10.1007/BF00160154. [DOI] [PubMed] [Google Scholar]
  43. Zuckerkandl E., Pauling L. Molecules as documents of evolutionary history. J Theor Biol. 1965 Mar;8(2):357–366. doi: 10.1016/0022-5193(65)90083-4. [DOI] [PubMed] [Google Scholar]
  44. Zuker M., Jacobson A. B. "Well-determined" regions in RNA secondary structure prediction: analysis of small subunit ribosomal RNA. Nucleic Acids Res. 1995 Jul 25;23(14):2791–2798. doi: 10.1093/nar/23.14.2791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zuker M., Jaeger J. A., Turner D. H. A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res. 1991 May 25;19(10):2707–2714. doi: 10.1093/nar/19.10.2707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 1989 Apr 7;244(4900):48–52. doi: 10.1126/science.2468181. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES